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Proof Only THE NAUTILUSProof 123(3):1–7, 2009 Only Page 1 (: ) associated with deep-water banks in the Mediterranean

Marco Taviani Mark Dimech Constantine Mifsud Lorenzo Angeletti University of Malta, St. Venera, Shepherds Street, Rabat RBT 02, ISMAR-CNR, Via Gobetti 101 MALTA MALTA 40129 Bologna, ITALY [email protected] [email protected] [email protected] [email protected]

Andre´ Freiwald M.G. Harasewych Marco Oliverio GZN-Geozentrum Nordbayern National Museum of Natural History, Dipartimento di Biologia Animale University of Erlangen, Smithsonian Institution e dell’Uomo GERMANY P.O. Box 37012 “La Sapienza” Rome University [email protected] Washington, DC 20013-7012 USA Viale dell’Universita` 32, [email protected] I-00185 Roma, ITALY [email protected]

ABSTRACT Unravelling the interactions between cnidarians and their predators is essential for a better understanding Fisheries and scientific investigations of the recently discov- of the ecology of deep-water coral banks. Top preda- ered deep-water coral province south of Malta sampled living tors of cnidarians include gastropods belonging to the specimens of two deep-water Coralliophilinae intimately asso- ciated with Lophelia-Madrepora coral banks. The species are families Ovulidae, Epitoniidae, Janthinidae, Muricidae- ‘’ richardi (Fischer P., 1882) and Coralliophilinae, and Architectonicidae (Graham, 1985; sentix (Bayer, 1971). A third coralliophilinid ‘Coralliophila’ Oliverio, 1989; Bieler & Petit, 2005; Schiaparelli et al., squamosa (Bivona Ant. in Bivona And., 1838: deep-water mor- 2005; Gittenberger, 2006, with references). However, photype) has been also observed alive close to deep-water there are few documented reports of gastropod preda- at the Nameless-Urania Bank. tion on Mediterranean deep-water corals due to: (1) the Additional keywords:, , XXXXX relative paucity of deep-water corals living in this basin, (2) the rarity of most coral-associated gastropod taxa, and (3) the inherent difficulties in imaging or sampling these deep-water habitats. Maltese, Italian, and German oceanographic cruises INTRODUCTION (Figure 1), sampled three rare deep-water Coralliophili- F1 dwc Deep-water coral ecosystems are receiving increasing nae at deep-water coral ( ) sites in the Strait of Sicily: ‘Coralliophila’ richardi (Fischer P., 1882), Babelomurex attention from the scientific community as biodiversity sentix ‘Coralliophila’ squamosa hotspots (Freiwald et al., 2004; Roberts et al., 2006). The (Bayer, 1971), and (Bivona Ant. in Bivona And., 1838: morphotype better Mediterranean Sea hosts a variety of deep-water corals ruderatus inhabiting soft and hard substrates. Some skeletonized known as Sturany, 1896) res- Lophelia pertusa pectively. The present report documents these findings cnidarians (mostly the scleractinians T1 (Linnaeus, 1758), Madrepora oculata Linnaeus, 1758; (Table 1). Desmophyllum dianthus (Esper, 1794), Javania cail- leti (Duchassaing and Michelotti, 1864), Caryophyllia spp., Dendrophyllia spp., the gorgoniacean Corallium CORALLIOPHILINES FROM MEDITERRANEAN rubrum (Linnaeus, 1758), and several others) may con- DEEP-WATER CORAL SITES tribute to the formation of considerable bioconstruc- ‘Coralliophila’ richardi (Fischer P., 1882) tions at depths in excess of 300 m (Taviani et al., 2005; Freiwald et al., 2009). Such living deep-water coral Murex richardi Fischer P., 1882: 49 assemblages are widespread in the Mediterranean basin Coralliophila lactuca Dall, 1889: 220, pl. 16, fig. 6 as are still-submerged taphocoenoses and outcrops Coralliophila richardi.—Bouchet and Ware´n, 1985: 152, (Taviani et al., 2005).Prooffig. Only 368 Page 2 Proof OnlyTHE NAUTILUS, Vol. 123, No. 3 Alboran Seas (Cecalupo, 1984; Oliverio, 1989; Giusti, 1996; Giannuzzi-Savelli et al., 2003). It also occurs as an Early Pleistocene fossil in deep-water deposits of pre- sumed Sicilian age in southern Italy (Vazzana, 1996). The taxonomic affinities of ‘Coralliophila’ richardi are obscure. The shell morphology of this species is unusual within the subfamily Coralliophilinae, and is shared only with Emozamia licinus (Hedley and Petterd, 1906), a deep-water, western Pacific species. Genetic studies of Mediterranean (this material) and Atlantic specimens will certainly elucidate the taxono- my of this group. The consistent co-occurence of Coralliophila. richardi with the scleractinians Lophelia and Madrepora in Recent and pre-modern assemblages has led to the suggestion that this taxon is likely a predator of one or Figure 1. Map showing station localities discussed in this both corals (e.g., Taviani and Colantoni, 1979). The reg- report. Symbols: h, live Coralliophila richardi (from literature ularly arched shape and dimension of the shell aperture and this paper); Š, subfossil C. richardi (from literature and of C. richardi seem well adapted for a sedentary position this paper); △, Babelomurex sentix; , ‘Coralliophila’ squa- on a branching stony coral colony such as those of mosa (morphotype ruderatus), •, subfossil ‘Coralliophila’ cf. Madrepora or Lophelia. squamosa (morphotype ruderatus). This hypothesis is supported by the co-occurence of live Lophelia, Madrepora, and C. richardi off Malta, the Remarks: Two living specimens of ‘Coralliophila’ latter fouled by juvenile Lophelia corals (Figures 5–6). F2 6 richardi (Figures 2–6) were trawled from Lophelia- Information from Atlantic Ocean specimens further sup- Madrepora coral banks off Malta during the GRUND ports the hypothesis of a strict relationship between C. 2003 mission (see Schembri et al., 2007). Additional pre- richardi and branching deep-water corals. A specimen F7 9 modern material (Figures 79; most likely glacial Pleisto- was photographed still adhering to the surface of living 0 cene fossils) was collected over many decades of sampling Lophelia on the Galicia Bank (Figure 19) (42 48.37 N, 0 during the CNR-Bologna oceanographic missions of the 11 47.47 W, 880 m depth). Coralliophila richardi has research vessels BANNOCK (see Bouchet and Ware´n, 1985; also been reported from various seamounts in the east- Taviani and Taviani, 1986) and URANIA (this study). ern Atlantic (Oliverio and Gofas, 2006), where it co- Coralliophila richardi (described from the Bay of Bis- occurs with living or dead coral (mostly Madrepora: cay) is the senior synonym of Coralliophila lactuca Dall, Gofas, unpublished notes, and M.T., unpublished 1889 (from off Cuba and Fernandina, Florida in the notes). In the western Atlantic, three live specimens of Western Atlantic: Bouchet and Ware´n, 1985; Taviani C. richardi were collected with living corals on a Lophe- and Taviani, 1986). This amphi-Atlantic species is now lia lithoherm (peak # 160) off St. Augustine, Florida 0 0 known from various sites in the eastern Atlantic Ocean (29 50.9726 N, 79 37.5976 W, in 871–746 m, bottom (Rolan and Pedrosa, 1981; Oliverio and Gofas, 2006) temperature 7.96 C; salinity 35.1) during dive JSL-I- and has been reported living in the Tyrrhenian and 4912 (Chief Scientist J. Reed), 11 Nov. 2005.

Table 1. Main attributes of stations yielding the Mediterranean coralliophilines discussed in the text.

Start End Sample Start Start Lat. Depth End Long Depth Cruise no. Area Long. N E (m) N End Lat E (m) Species 0 0 0 0 CS73 7 Nameless Urania 36 53.600 13 06.300 695 36 51.800 13 06.300 410 Coralliophila Bank richardi 0 0 0 0 ET95 D21 Tuscan Archip. 43 18.850 09 48.920 582 43 19.450 09 49.080 515 C. richardi 0 0 0 0 GRUND2003 G19 Malta 35 30.47 14 06.27 617 35 30.830 14 06.020 420 C. richardi 0 0 0 0 MARCOS MS43 Malta 35 30.720 14 06.561 607 35 30.803 14 06.511 452 Babelomurex sentix 0 0 0 0 MARCOS MS44 Malta 35 30.506 14 06.230 632 35 31.228 14 05.698 467 B. sentix 0 0 0 0 CORTI CORTI71 Tuscan 43 13.505 09 36.326 369 43 13.682 09 36.260 399 Coralliophila Archipelago squamosa (morphotype ruderatus) 0 0 0 0 M70-1 677 NamelessUrania 36 50.340 13 09.300 544 36 50.340 13 09.390 388 C. squamosa Bank (morphotype Proof Onlyruderatus) Marco Taviani etProof al., 2009 Only Page 3

Figures 2–9. Coralliophila richardi. 2–6. Living Coralliophila richardi from Malta coral banks (st. GRUND 2003-G19). 2–4. Sinuous outer lip accommodates settlement on coral branch. Scale bar = 1 cm. 5–6. Fouling by scleractinian corals (e.g., Lophelia pertusa: A, Vertino, pers, comm.. 2008) and barnacles. Scale bar = 1 cm. 7–9. Specimens from Pleistocene submerged assemblages. 7–8. Strait of Sicily (Station CS73-7). Scale bar = 1 cm. 9. Tuscan Archipelago (Station ET95-D21). Scale bar = 1 cm. Proof Only Page 4 Proof OnlyTHE NAUTILUS, Vol. 123, No. 3 Coralliophila richardi also occurs in the Gulf of Mex- their expanded soft parts (Figures 18–20). Its presumed F18 20 ico on live deep-water coral banks. Norem et al. (2008: association with white corals (Oliverio, 1989) is only pl. 27B) illustrated two specimens of C. richardi (identi- based on indirect evidence. C. abbreviata fied as the shallow-water (Lamarck, Coralliophila squamosa 1816)), on live coral from the Lophelia banks of the (Bivona Ant. in Bivona And., Viosca Knoll in circa 315 m depth (dive JSL 4747). 1838) Fusus squamosus Babelomurex sentix (Bayer, 1971) Bivona Ant. in Bivona And., 1838: 14; fig. 22 Coralliophila sentix Bayer, 1971: 189, fig. 49 Murex alucoides Blainville, 1829: 128; pl. 5B fig. 1 (non sentix carcassii Nicolay and Angioy, 1985: 16–18 Murex alucoides Olivi 1792) Fusus lamellosus Babelomurex sentix Philippi, 1836 [ex de Cristofori and Jan Remarks: (originally described ms.]: 204–205, pl. 11 fig. 30 (non Fusus lamellosus Bor- from east of St. Vincent, Lesser Antilles) is a rare amphi- son 1821) Atlantic species seldom found alive (Bayer, 1971; Oliverio Fusus squamulosus Philippi, 1836: 204, pl. 11 fig. 31 and Gofas, 2006). There are a few scattered records from (non Fusus squamulosus Deshayes, 1835) the western basin of the Mediterranean Sea off Sardinia, ? Pseudomurex perfectus Fischer P., 1883: 274 Melilla, and Alboran. Within this basin, fresh shells, inclu- ? Pseudomurex ruderatus Sturany, 1896 [ex Monterosato ding some with , document that this species has ms.]; 26, pl. 2 fig. 42–43 been found alive in the Mediterranean more than once ? Pseudomurex monterosatoi Latiaxis sentix carcassii Locard, 1897: 315, pl. 15 (Nikolay and Angioy, 1985: as ; fig. 21–23 Oliverio, 1989; Giannuzzi-Savelli et al., 2003). F10 12 Two living specimens (Figures 10–12) and one shell of Remarks: ‘Coralliophila’ squamosa (originally des- Babelomurex sentix were trawled from south of Malta cribed from Sicily, but currently with a neotype from from coral banks dominated by adult Lophelia, Madre- Corsica: Bouchet and Waren, 1985), is a relatively pora, and Desmophyllum and small colonies of Coral- common and widespread taxon known throughout the lium in 2007 during the MARCOS cruise (Chief Mediterranean Sea. It is presumed to be associated with Scientist Marco Taviani). The were kept alive in gorgonians, and, on the deeper continental shelf, with the aquarium onboard the ship for a week and were scleractinians (Oliverio, 1989), although there is no di- quite active, thus permitting a full documentation of rect evidence for this.

Figures 10–12. Living specimens of Babelomurex sentix collected from Malta deep-water coral banks during the MARCOS cruise (Station MS43). ScaleProof bar = 1 cm. Only Marco Taviani etProof al., 2009 Only Page 5 A plausible association of C. squamosa, recorded as sentix and C. squamosa (morphotype ruderatus)seem larger and smoother morphotypes of Coralliophila confined to deep water coral banks, but their precise hosts lamellosa (de Cristofori and Jan, 1832), with Mediterra- have yet to be identified. The supraspecific position of nan deep-water corals was reported by Taviani and these three bathyal coralliophilines is still unclear. Colantoni (1979). These shells are included in Pseudo- Recent collections of living specimens of these rare murex ruderatus (Sturany, 1896). Pseudomurex rudera- Coralliophilinae have provided material for molecular sys- tus may represent a deep-water morphotype of the tematic studies, as well as for determination of their host variable Atlantic-Mediterranean ‘Coralliophila’ squa- cnidarians through DNA barcoding of their gut contents mosa and their mutual relationships will be elucidated (Oliverio and Mariottini, 2001; Oliverio et al., 2009). by an on-going genetic study. The biogeography of these very rare coralliophilines A single live individual of ‘Coralliophila’ squamosa merits attention. For all three species, connections be- F13 14 (morphotype ruderatus: Figures 13–14) has been photo- tween Mediterranean and Atlantic populations may be graphed and then collected using the MARUM ROV linked to their supposedly teleplanic larvae. All three QUEST 4000 M during cruise M70-1 of R/V METEOR species (C. squamosa, C. richardi, and B. sentix) have (Chief Scientist A. Freiwald). A single living specimen established populations in the Atlantic Ocean. Their (Figure 17) was found on the volcanic bedrock at circa planktotrophic larvae may have been passively dispersed 500 m off the Nameless-Urania Bank, Strait of Sicily. into the Mediterranean by currents. This may have led The ROV images document a variety of co-occurring to the establishment of viable populations in this basin cnidarians at this site including Lophelia, Madrepora, (as it is certainly the case for C. squamosa) although Desmophyllum, Corallium, as well as antipatharians and the possibility of non-reproductive pseudo-populations gorgonians. Other empty shells collected from various (Bouchet and Taviani, 1992) can not be ruled out. How- deep-water sites in the Mediterranean basin may also ever, Coralliophila squamosa is not uncommon (with its F15 belong to this elusive taxon (Figure 15). typical morphotypes) in shallower waters throughout its range, and the rarity of its putative deep-water morpho- type ruderatus may be related to sampling difficulties. Coralliophila richardi CONCLUSIONS is known from multiple sites in the western Mediterranean and this suggests a status of Of the coralliophilines associated with deep-water coral permanent resident in the basin, also supported by its banks, Coralliophila richardi is strictly associated with prolonged, albeit not necessarily continuous, presence Lophelia and very likely with Madrepora. Babelomurex in this basin since the Early Pleistocene. Records of

Figures 13–15. Coralliophila’ squamosa (morphotype ruderatus). 13–14. Live-collected specimen from the Nameless-Urania bank, Strait of Sicily, Station M70/1-677. 15. Shell from a Pleistocene submerged assemblage, Tuscan Archipelago, Station CORTI- 71. Scale bar = 1Proof cm. Only Page 6 Proof OnlyTHE NAUTILUS, Vol. 123, No. 3

Figures 16–20. Living Coralliophila richardi. 16. Live specimen on living Lophelia pertusa, Galicia Bank. Scale bar = 3 mm. 17. In situ photograph of ‘Coralliophila’ squamosa (morphotype ruderatus) recovered from the Nameless-Urania Bank (Station. M70/1-677). Scale bar = 5 mm. 18–20. Babelomurex sentix with extended soft parts, collected during the MARCOS cruise. 18, 20. Adult specimen from StationMS44. 19. Immature specimen from Station MS43. Scale bar = 1cm.

B. sentix in the Mediterranean Sea are scanty. Further Ceregato helped with samples and bibliography. Partial evidence is the needed for us to demonstrate the pres- funding provided by FP-VI Integrated Project HERMES ence of permanent populations in the region. (GOCE-CT-2005-511234-1) and HERMIONE of the European Commission and by BIOCORAL grant (Minis- try of Environment of Italy). This is ISMAR-CNR scientific ACKNOWLEDGMENTS contribution no. 1633. For their cooperation, we are grateful to Captains, crew, and scientific staff of R/V URANIA during the MARCOS LITERATURE CITED cruise, of R/V VICTOR HENSEN cruise VH-97, and R/V METEOR cruise M70/1 for their cooperation. Lydia Bayer, F. M. 1971. Biological results of the University of Miami Beuck, GZN-Erlangen, assisted with GIS positioning and Deep-Sea expeditions. 79. New and unusual mollusks col- archiving of M70/1Proof data. 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